Solid-State NMR Studies Reveal Native-like β-Sheet Structures in Transthyretin Amyloid

Lim, Kwang Hun; Dasari, Anvesh K. R.; Hung, Ivan; Gan, Zhehong; Kelly, Jeffery W.; Wright, Peter E.; Wemmer, David E.

doi:10.1021/acs.biochem.6b00649

Title: Solid-State NMR Studies Reveal Native-like β-Sheet Structures in Transthyretin Amyloid

Journal Article · Fri Sep 02 00:00:00 EDT 2016 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.6b00649· OSTI ID:1377496

Lim, Kwang Hun ^[1]; Dasari, Anvesh K. R. ^[1]; Hung, Ivan ^[2]; Gan, Zhehong ^[2]; Kelly, Jeffery W. ^[3]; Wright, Peter E. ^[3]; Wemmer, David E. ^[4]

East Carolina Univ., Greenville, NC (United States)
National High Magnetic Field Lab. (NHMFL), Tallahassee, FL (United States)
Scripps Research Inst., La Jolla, CA (United States)
Univ. of California, Berkeley, CA (United States)

Structural characterization of amyloid rich in cross-β structures is crucial for unraveling the molecular basis of protein misfolding and amyloid formation associated with a wide range of human disorders. Elucidation of the β-sheet structure in noncrystalline amyloid has, however, remained an enormous challenge. Here we report structural analyses of the β-sheet structure in a full-length transthyretin amyloid using solid-state NMR spectroscopy. Magic-angle-spinning (MAS) solid-state NMR was employed to investigate native-like β-sheet structures in the amyloid state using selective labeling schemes for more efficient solid-state NMR studies. Analyses of extensive long-range 13 C- 13 C correlation MAS spectra obtained with selectively 13 CO- and 13 Cα-labeled TTR reveal that the two main β-structures in the native state, the CBEF and DAGH β-sheets, remain intact after amyloid formation. The tertiary structural information would be of great use for examining the quaternary structure of TTR amyloid.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: East Carolina Univ., Greenville, NC (United States); Scripps Research Inst., La Jolla, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; National Inst. of Health (NIH) (United States); National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231; NS084138; DK34909; AG10770; DK46335; DMR-1157490

OSTI ID:: 1377496

Journal Information:: Biochemistry, Vol. 55, Issue 37; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 25 works

Citation information provided by
Web of Science

References (43)

Protein folding and misfolding Dobson, Christopher M. Nature, Vol. 426, Issue 6968 https://doi.org/10.1038/nature02261	journal	December 2003
Molecular structure of amyloid fibrils: insights from solid-state NMR Tycko, Robert Quarterly Reviews of Biophysics, Vol. 39, Issue 1 https://doi.org/10.1017/S0033583506004173	journal	February 2006
From the globular to the fibrous state: protein structure and structural conversion in amyloid formation Sunde, Margaret; Blake, Colin C. F. Quarterly Reviews of Biophysics, Vol. 31, Issue 1 https://doi.org/10.1017/S0033583598003400	journal	February 1998
The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways Kelly, Jeffery W. Current Opinion in Structural Biology, Vol. 8, Issue 1 https://doi.org/10.1016/S0959-440X(98)80016-X	journal	February 1998
Folding versus aggregation: Polypeptide conformations on competing pathways Jahn, Thomas R.; Radford, Sheena E. Archives of Biochemistry and Biophysics, Vol. 469, Issue 1 https://doi.org/10.1016/j.abb.2007.05.015	journal	January 2008
The Acid-Mediated Denaturation Pathway of Transthyretin Yields a Conformational Intermediate That Can Self-Assemble into Amyloid ^† Lai, Zhihong; Colón, Wilfredo; Kelly, Jeffery W. Biochemistry, Vol. 35, Issue 20 https://doi.org/10.1021/bi952501g	journal	January 1996
Transthyretin mutations in health and disease João, Maria; Saraiva, Mascarenhas Human Mutation, Vol. 5, Issue 3 https://doi.org/10.1002/humu.1380050302	journal	January 1995
Amyloid formation by globular proteins under native conditions Chiti, Fabrizio; Dobson, Christopher M. Nature Chemical Biology, Vol. 5, Issue 1 https://doi.org/10.1038/nchembio.131	journal	December 2008
Amyloid Formation by Human Carboxypeptidase D Transthyretin-like Domain under Physiological Conditions Garcia-Pardo, Javier; Graña-Montes, Ricardo; Fernandez-Mendez, Marc Journal of Biological Chemistry, Vol. 289, Issue 49 https://doi.org/10.1074/jbc.M114.594804	journal	October 2014
A model for the aggregation of the acylphosphatase from Sulfolobus solfataricus in its native-like state Bemporad, Francesco; Vannocci, Tommaso; Varela, Lorena Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12 https://doi.org/10.1016/j.bbapap.2008.08.021	journal	December 2008
Folding of Cu/Zn superoxide dismutase suggests structural hotspots for gain of neurotoxic function in ALS: Parallels to precursors in amyloid disease Nordlund, A.; Oliveberg, M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 27 https://doi.org/10.1073/pnas.0601696103	journal	June 2006
Amyloid Formation of a Protein in the Absence of Initial Unfolding and Destabilization of the Native State Soldi, Gemma; Bemporad, Francesco; Torrassa, Silvia Biophysical Journal, Vol. 89, Issue 6 https://doi.org/10.1529/biophysj.105.067538	journal	December 2005
Amyloid formation under physiological conditions proceeds via a native-like folding intermediate Jahn, Thomas R.; Parker, Martin J.; Homans, Steve W. Nature Structural & Molecular Biology, Vol. 13, Issue 3 https://doi.org/10.1038/nsmb1058	journal	February 2006
Structure of prealbumin: Secondary, tertiary and quaternary interactions determined by Fourier refinement at 1.8 Å Blake, C. C. F.; Geisow, M. J.; Oatley, S. J. Journal of Molecular Biology, Vol. 121, Issue 3 https://doi.org/10.1016/0022-2836(78)90368-6	journal	May 1978
Probing Solvent Accessibility of Transthyretin Amyloid by Solution NMR Spectroscopy Olofsson, Anders; Ippel, Johannes H.; Wijmenga, Sybren S. Journal of Biological Chemistry, Vol. 279, Issue 7 https://doi.org/10.1074/jbc.M310605200	journal	November 2003
A glimpse of a possible amyloidogenic intermediate of transthyretin Liu, Kai; Cho, Ho S.; Lashuel, Hilal A. Nature Structural Biology, Vol. 7, Issue 9, p. 754-757 https://doi.org/10.1038/78980	journal	January 2000
Arrangement of subunits and ordering of β-strands in an amyloid sheet Serag, Ahmed A.; Altenbach, Christian; Gingery, Mari Nature Structural Biology, Vol. 9, Issue 10 https://doi.org/10.1038/nsb838	journal	September 2002
Experimentally Derived Structural Constraints for Amyloid Fibrils of Wild-Type Transthyretin Bateman, David A.; Tycko, Robert; Wickner, Reed B. Biophysical Journal, Vol. 101, Issue 10 https://doi.org/10.1016/j.bpj.2011.10.009	journal	November 2011
Localized Structural Fluctuations Promote Amyloidogenic Conformations in Transthyretin Lim, Kwang Hun; Dyson, H. Jane; Kelly, Jeffery W. Journal of Molecular Biology, Vol. 425, Issue 6 https://doi.org/10.1016/j.jmb.2013.01.008	journal	March 2013
Structural Changes Associated with Transthyretin Misfolding and Amyloid Formation Revealed by Solution and Solid-State NMR Lim, Kwang Hun; Dasari, Anvesh K. R.; Hung, Ivan Biochemistry, Vol. 55, Issue 13 https://doi.org/10.1021/acs.biochem.6b00164	journal	March 2016
High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy Jaroniec, C. P.; MacPhee, C. E.; Bajaj, V. S. Proceedings of the National Academy of Sciences, Vol. 101, Issue 3 https://doi.org/10.1073/pnas.0304849101	journal	January 2004
A low-E magic angle spinning probe for biological solid state NMR at 750MHz McNeill, Seth A.; Gor’kov, Peter L.; Shetty, Kiran Journal of Magnetic Resonance, Vol. 197, Issue 2 https://doi.org/10.1016/j.jmr.2008.12.008	journal	April 2009
Rotational resonance in solid state NMR Raleigh, D. P.; Levitt, M. H.; Griffin, R. G. Chemical Physics Letters, Vol. 146, Issue 1-2 https://doi.org/10.1016/0009-2614(88)85051-6	journal	April 1988
Protein solid-state NMR resonance assignments from (13C,13C) correlation spectroscopy Seidel, Karsten; Lange, Adam; Becker, Stefan Physical Chemistry Chemical Physics, Vol. 6, Issue 22 https://doi.org/10.1039/b411689e	journal	January 2004
Transthyretin Aggregation under Partially Denaturing Conditions Is a Downhill Polymerization ^† Hurshman, Amy R.; White, Joleen T.; Powers, Evan T. Biochemistry, Vol. 43, Issue 23 https://doi.org/10.1021/bi049621l	journal	June 2004
Advanced Solid-State NMR Approaches for Structure Determination of Membrane Proteins and Amyloid Fibrils Tang, Ming; Comellas, Gemma; Rienstra, Chad M. Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar4000168	journal	May 2013
Molecular Structure of β-Amyloid Fibrils in Alzheimer’s Disease Brain Tissue Lu, Jun-Xia; Qiang, Wei; Yau, Wai-Ming Cell, Vol. 154, Issue 6 https://doi.org/10.1016/j.cell.2013.08.035	journal	September 2013
Higher Order Amyloid Fibril Structure by MAS NMR and DNP Spectroscopy Debelouchina, Galia T.; Bayro, Marvin J.; Fitzpatrick, Anthony W. Journal of the American Chemical Society, Vol. 135, Issue 51 https://doi.org/10.1021/ja409050a	journal	December 2013
Amyloid Fibrils of the HET-s(218-289) Prion Form a Solenoid with a Triangular Hydrophobic Core Wasmer, C.; Lange, A.; Van Melckebeke, H. Science, Vol. 319, Issue 5869 https://doi.org/10.1126/science.1151839	journal	March 2008
Intermolecular Alignment in Y145Stop Human Prion Protein Amyloid Fibrils Probed by Solid-State NMR Spectroscopy Helmus, Jonathan J.; Surewicz, Krystyna; Apostol, Marcin I. Journal of the American Chemical Society, Vol. 133, Issue 35 https://doi.org/10.1021/ja206469q	journal	September 2011
Proton-Detected Solid-State NMR Spectroscopy of Fibrillar and Membrane Proteins Linser, Rasmus; Dasari, Muralidhar; Hiller, Matthias Angewandte Chemie International Edition, Vol. 50, Issue 19 https://doi.org/10.1002/anie.201008244	journal	April 2011
Fibrillar vs Crystalline Full-Length β-2-Microglobulin Studied by High-Resolution Solid-State NMR Spectroscopy Barbet-Massin, Emeline; Ricagno, Stefano; Lewandowski, Józef R. Journal of the American Chemical Society, Vol. 132, Issue 16 https://doi.org/10.1021/ja1002839	journal	April 2010
β-Sheet Core of Tau Paired Helical Filaments Revealed by Solid-State NMR Daebel, Venita; Chinnathambi, Subashchandrabose; Biernat, Jacek Journal of the American Chemical Society, Vol. 134, Issue 34 https://doi.org/10.1021/ja305470p	journal	August 2012
Magic-Angle-Spinning NMR Techniques for Measuring Long-Range Distances in Biological Macromolecules Hong, Mei; Schmidt-Rohr, Klaus Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar300294x	journal	February 2013
Probing Structure and Dynamics of Protein Assemblies by Magic Angle Spinning NMR Spectroscopy Yan, Si; Suiter, Christopher L.; Hou, Guangjin Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar300309s	journal	February 2013
Structural Insight into an Alzheimer’s Brain-Derived Spherical Assembly of Amyloid β by Solid-State NMR Parthasarathy, Sudhakar; Inoue, Masafumi; Xiao, Yiling Journal of the American Chemical Society, Vol. 137, Issue 20 https://doi.org/10.1021/jacs.5b03373	journal	May 2015
Solid-State NMR-Based Approaches for Supramolecular Structure Elucidation Weingarth, Markus; Baldus, Marc Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar300316e	journal	April 2013
Observation of spin exchange by two-dimensional fourier transform 13C cross polarization-magic-angle spinning Szeverenyi, Nikolaus M.; Sullivan, Mark J.; Maciel, Gary E. Journal of Magnetic Resonance (1969), Vol. 47, Issue 3 https://doi.org/10.1016/0022-2364(82)90213-X	journal	May 1982
Magic Angle Spinning NMR Analysis of β ₂ -Microglobulin Amyloid Fibrils in Two Distinct Morphologies Debelouchina, Galia T.; Platt, Geoffrey W.; Bayro, Marvin J. Journal of the American Chemical Society, Vol. 132, Issue 30 https://doi.org/10.1021/ja102775u	journal	August 2010
Conformational Flexibility of Y145Stop Human Prion Protein Amyloid Fibrils Probed by Solid-State Nuclear Magnetic Resonance Spectroscopy Helmus, Jonathan J.; Surewicz, Krystyna; Surewicz, Witold K. Journal of the American Chemical Society, Vol. 132, Issue 7 https://doi.org/10.1021/ja909827v	journal	February 2010
A comparative analysis of 23 structures of the amyloidogenic protein transthyretin Hörnberg, Andreas; Eneqvist, Therese; Olofsson, Anders Journal of Molecular Biology, Vol. 302, Issue 3 https://doi.org/10.1006/jmbi.2000.4078	journal	September 2000
Conformational differences between the wild type and V30M mutant transthyretin modulate its binding to genistein: Implications to tetramer stability and ligand-binding Trivella, Daniela B. B.; Bleicher, Lucas; Palmieri, Leonardo de Castro Journal of Structural Biology, Vol. 170, Issue 3 https://doi.org/10.1016/j.jsb.2010.03.002	journal	June 2010
Considerably Unfolded Transthyretin Monomers Preceed and Exchange with Dynamically Structured Amyloid Protofibrils Groenning, Minna; Campos, Raul I.; Hirschberg, Daniel Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep11443	journal	June 2015

Cited By (4)

Transthyretin Aggregation Pathway toward the Formation of Distinct Cytotoxic Oligomers Dasari, Anvesh K. R.; Hughes, Robert M.; Wi, Sungsool Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-37230-1	journal	January 2019
Studies of the Process of Amyloid Formation by Aβ Peptide Galzitskaya, O. V.; Galushko, E. I.; Selivanova, O. M. Biochemistry (Moscow), Vol. 83, Issue S1 https://doi.org/10.1134/s0006297918140079	journal	January 2018
Cryo-EM structure of a transthyretin-derived amyloid fibril from a patient with hereditary ATTR amyloidosis Schmidt, Matthias; Wiese, Sebastian; Adak, Volkan Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13038-z	journal	November 2019
Atomic force microscopy for single molecule characterisation of protein aggregation Ruggeri, Francesco Simone; Šneideris, Tomas; Vendruscolo, Michele Archives of Biochemistry and Biophysics, Vol. 664 https://doi.org/10.1016/j.abb.2019.02.001	journal	March 2019

Similar Records

Structural Changes Associated with Transthyretin Misfolding and Amyloid Formation Revealed by Solution and Solid-State NMR

Journal Article · Mon Mar 21 00:00:00 EDT 2016 · Biochemistry · OSTI ID:1377496

Lim, Kwang Hun; Dasari, Anvesh K. R.; Hung, Ivan; +3 more

Prefibrillar transthyretin oligomers and cold stored native tetrameric transthyretin are cytotoxic in cell culture

Journal Article · Fri Dec 26 00:00:00 EST 2008 · Biochemical and Biophysical Research Communications · OSTI ID:1377496

Soergjerd, Karin; Klingstedt, Therese; Lindgren, Mikael; +2 more

A Substructure Combination Strategy To Create Potent and Selective Transthyretin Kinetic Stabilizers That Prevent Amyloidogenesis and Cytotoxicity

Journal Article · Fri Aug 13 00:00:00 EDT 2010 · J. Am. Chem. Soc. · OSTI ID:1377496

Choi, Sungwook; Reixach, Natlia; Connelly, Stephen; +3 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Title: Solid-State NMR Studies Reveal Native-like β-Sheet Structures in Transthyretin Amyloid

Citation Formats

References (43)

Cited By (4)

Similar Records

Related Subjects